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Файл:Ординатура / Хирургия / Библиотека им академика М.И. Перельмана / Книга_103_библиотеки_им_акад_М_И_Перельмана
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32.2.1 Recording Equipment
32.2.1.1 Electrodes
Electrodes to record the VEP are typically Cl-Clchloride, gold cup, or surface electrodes applied
to the occipital scalp. According to the international 10–20 system, at a minimum, the electrode
should be placed at the mid-occiput (Oz) and is
typically referred to as the mid-frontal region
(Fz), with a ground placed around the central
scalp (Cz), to record a single channel VEP. As
these are a minimum requirement, additional
electrodes placed laterally (i.e., O1/O2, or even
T5/T6) can be used to identify the contributions
from each hemisphere to a stimulus. The latter is
useful in evaluating hemianopic or bi-temporal/
bi-nasal eld decits [3]. Furthermore, in pediatric practice, an electrode placed inferiorly to the
Oz over the inion (Iz) provides larger amplitudes
for those under 8 years of age for a standard
check width (50′) and for those under 12years of
age for a small check width (12.5′) [4]. An illustration of these electrode positions is seen in
Fig.32.1.
Before applying the electrodes, the application site should be prepared using an abrasive gel.
This is typically performed using a cotton tip,
which can also be used to part the hair, depending
on the location. Electrode impedance (measured
by passing a low voltage signal through the electrodes to observe their respective resistance)
should then be measured to ensure that these are
balanced (typically within 20%) and maintained
below 5 kOhms. It is the author’s practice to wrap
a Coban strip around the electrode sites following
electrode application to minimize movement
(including coiling of wires) and potential shift of
electrodes during testing to minimize external
noise intrusion.
32.2.1.2 Signal Acquisition
The VEP is a time-locked subtraction of the
background electroencephalographic signal. As
such, this is an analog signal arising from cortical
neurons. Modern systems require digitization of
the signals to enable processing on software and
potential post-hoc analysis or modication. To
achieve this, the incoming ongoing electro-
Fig. 32.1 Illustration of electrode positions for the
VEP.Electrodes are placed according to positions dened
in the international 10–20 system. The left illustration
shows the side view of the head, with active electrodes positioned at Oz (middle of the occiput), Iz (inion), with the
reference electrode placed anteriorly over Fz (mid- frontal)
and ground around the center of the head (Cz). The posterior view of the head shows the multichannel VEP electrode
array, with the Oz and Iz electrodes, but also lateral electrodes placed over the left (O1) and right (O2) occiput
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graphic signal is sampled at a high rate (at a minimum, twice the frequency of the signal of interest
according to the Nyquist-Shannon theorem) in
the order of <1kbps. All signals will have a form
of differential amplication of the signal prior to
signal analysis.
Differential ampliers work in a manner
whereby the difference between two inputs is calculated. Therefore, a large signal in one electrode
and a minimal signal in another will produce a
large amplitude output. An example of this would
be the Oz electrode being an active electrode over
the visual cortex and the Fz electrode being a
relatively inactive electrode over the anterior
scalp; therefore, the VEP produced is due to a difference in signal strength between these electrodes. Signals of the same size and temporal
prole, when they enter both electrodes, are said
to be in common mode, which typically results in
minimal signal output and highlights the importance of balanced electrode inputs. The amplied
signals are then subject to ltering, typically used
to attenuate frequency bands, allowing one to
eliminate unwanted signals (i.e., noise). For the
VEP, this is typically set as a 0.3–100 Hz bandpass lter as per the ISCEV (International Society
for Clinical Electrophysiology of Vision)
standards.
The size of the incoming signal can be automatically rejected in some software programs by
determining a rejection criterion based on amplitude. For most instances, this is 100–200μV (signals above this are automatically rejected).
As the VEP is a time-locked signal of the
background electroencephalogram (EEG) signal, averaging is required to improve the signal–
noise ratio. Typically, 100 trials are used to
constitute an average response, which is then
repeated to demonstrate reproducibility. The
number of trials may be reduced in people with
poorer xation and compliance but should be
repeated to conrm the reproducibility of the
response.
32.2.1.3 Display andSoftware
Requirements
Display requirements for the analysis of the VEP
should allow analysis of the entire waveform on a
high-resolution monitor. The software should
enable measuring the peak-time and amplitude of
the VEP, ideally with enabled post-hoc manual or
automatic rejection of trials to improve the signal–noise ratio.
32.2.2 Stimuli
A VEP can theoretically be elicited to a variety
of visual stimuli, for example, color, motion,
contrast, luminance, or in some circumstances,
an event related to particular stimuli. Despite
this, the major clinical applications of the VEP
relate to luminance and contrast through the
ash (f-) and pattern reversal (pr-) or pattern
onset-offset (po-) stimuli, respectively.
Accordingly, there are ISCEV standards for
these ash and pattern stimuli [3].
The prVEP, poVEP, and f-VEP show different
waveforms, which are typically named according
to their respective polarity (P for positive and N
for negative), timing (i.e., P100= positivity at
100ms), or order of presentation (i.e., P1 or P2).
These waveforms are illustrated in Fig.32.2.
For patterned stimuli, there should be an
abrupt change of contrast at the stimulus onset
without any signicant alterations in mean luminance. This is easily achieved with the older
visual display units (VDU), such as plasma display panels or cathode-ray tube devices; however, at the time of writing, these devices are
obsolete and not widely manufactured.
Unfortunately, common alternatives such as liquid crystal display monitors are usually unsuitable as these have a detrimental luminance
artifact with pattern reversals [5, 6]. Modern
devices such as digital light projection (DLP)
systems or organic light-emitting diode (OLED)
devices may be able to overcome these issues, but
these are still under review [7, 8]. Any transient
luminance artifacts can be easily visualized by
darkening the room and placing a piece of paper
before the observer’s eyes, facing toward the
stimulus, to monitor for any transient luminance
alterations visually. Otherwise, these can be measured formally with a photodiode. Any individuals setting up laboratories should be aware of
these potential VDU limitations and their confounding effects on the PVEP or PERG.
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Fig. 32.2 Typical waveforms of the pattern electroretinogram (PERG), pattern reversal visual evoked potential
(prVEP), pattern onset-offset VEP (poVEP), and ash
Fig. 32.3 The effect of check width on the pattern reversal VEP.The gure on the left shows the waveform alterations with check width, with the top (large check) showing
the earliest peak-time, with the amplitude then showing an
The temporal frequency of the stimulus can
either be transient or steady-state. The former is
most common in clinical practice, as this allows
the isolation of individual waveform components, which can be measured for their peaktime, amplitudes, and shape to identify
dysfunction. Steady-state responses are those
recorded at higher temporal frequencies (typically >10Hz). These have been utilized in clinical practice with varying purposes; the most
commonly used is a sweep VEP to provide an
objective estimation of visual acuity [9].
The stimulus eld size should subtend at least
15° of the visual eld, typically viewed at around
1m, per the ISCEV VEP standards [3]. It is the
author’s practice to have a larger eld size, which
is advantageous for pediatric patients whose xation and eye position may be more variable; it is
VEP (f-VEP). The waveforms are plotted by amplitude
and time and labeled according to the conventional
nomenclature consistent with the ISCEV standards
inverse U-shaped function with decreasing check width,
with increasing peak-time. These data are plotted according to the check width in the right panel (amplitude in
blue, peak-time in red)
increased to around 30° to allow for variable xation. However, with increasing eld size, one
must be more aware of the alterations in the
prVEP morphology. Typically, with larger eld
sizes, there are larger contributions from
paramacular prVEP components, which is discussed later in this chapter.
Check width is an important factor for performing the VEP. The ISCEV VEP standard
species that the prVEP should be recorded with
a large (1°) and small (0.25°) check width.
Importantly, the amplitude typically shows an
inverse U-shaped function with the peak amplitude around 15 min of arc (0.25°), while the
amplitude shows a more linear increase with
decreasing check width (Fig. 32.3). Expanding
the number of check widths used in clinical practice can reveal macular pathway dysfunction
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where small check widths are affected rst [10]
and can give more consistency to a response.
Therefore, while a minimum of two check widths
should be used, additional check widths are benecial to characterize macular pathway function
in practice.
32.3 Technique
A typical recording setup would have a patient
seated comfortably in a chair, preferably with a
high back and headrest. Electrodes would be
applied with low, balanced impedances. During
application, a discussion on how the test is performed and what is needed from the patient can
be initiated, and any questions can be answered.
It is essential to ensure that the patient is relaxed
to minimize muscle artifacts (i.e., chewing, neck
straining, etc.) and ensure their comfort as best
possible (i.e., with neck pillows, adjustment of
seating position, etc.).
The patient should wear their most recent
spectacles for testing. If these are unavailable,
trial frames can be used, or if unavailable, a note
made in the report that the tests were performed
uncorrected (and dene their correction). The
pattern VEP can withstand a signicant degree of
optical blur but is dependent on test strategy and
other patient factors, the degree of which should
be noted.
For children, alternating the stimulus checkerboard with a video of their choosing will most
likely result in better testing conditions and a
happier child! The prVEP depends on xation
and attention; therefore, this should be monitored
closely for xation loss, deliberate mis-xation,
or xation drift. One way this can be achieved is
by simultaneously using camera systems (i.e.,
CCTV, IP cameras) to monitor the patient’s xation during signal acquisition. Thus, in periods of
xation loss, signal acquisition can be paused
and resumed once xation has returned. In
younger children, larger eld sizes are necessary
to attract attention and account for some unavoidable xation variance. In these circumstances, it
is best to work with colleagues as a pair, one to
“distract and interact” with the child and the
other to focus solely on signal acquisition.
Fixation can be encouraged using small toys or
ngers at the top of the stimulus screen. As the
prVEP is dominated by the inferior eld, small
obscurations in the superior eld have negligible
impacts on the PVEP and enable more reliable
xation on the stimulus. Intermittent averaging is
required to allow for the patient’s attention.
Prolonged presentation of a checkerboard stimulus will lead to tiredness, habituation, or defocus,
even in the most enthusiastic of adults.
32.4 Clinical Application
andInterpretation
The typical responses to ash, pattern reversal,
pattern onset-offset stimuli are illustrated in
Fig. 32.2. To interpret the VEP waveform, the
acronym “PAST” (Peak-time, Amplitude, Shape,
Transoccipital asymmetry) can be used to evaluate the response.
32.4.1 Peak-Time
The peak-time of the waveform signies the time
taken for cortical activation following afferent
pathway stimulation. The peak-time is most conventionally measured from the major positive
peak of the respective VEP waveform, for example, the P100 of the prVEP, C1 of the poVEP, and
P2 of the ash VEP [3]. A delay in peak-time
(i.e., a peak-time exceeding the laboratory reference range) can result from dysfunction of the
physiological substrates underlying the response.
For example, a delay of the prVEP P100 can be
due to a dysfunction of the macular, retinal
ganglion cells, optic nerve, or chiasmal/retro chiasmal visual pathway. To elaborate on the dysfunction site, a PERG is required to delineate
between macular, retinal ganglion cell, or optic
nerve/pathway dysfunction. While prVEPs to
standard check widths are fairly resistant to an
optical blur of <5 D, the interpretation of peaktime delays to smaller check widths must be cautiously made, as this may result from uncorrected
refractive error, reduced contrast (i.e., from anterior segment disease such as cataract) or poor
xation/blurring. Another important consider-
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ation is the maturation of the VEP.The VEP to
standard (large) check widths is typically within
10% of adult peak-times by 6months of age, but
younger people may have longer peak-times due
to the immaturity of their visual pathways.
Similarly, poVEPs can show shape-dependent
changes with maturation [11]. This is an important consideration for interpreting the PVEP, as
these factors should be excluded before attributing a peak-time delay to macular pathway dysfunction, including age-matched reference data.
Simultaneous PERG and PVEP recordings can
elaborate on an abnormal VEP, particularly for
suspected optical blur or defocus, as the PERG is
far more sensitive to uncorrected refractive error
and contrast alterations [12].
Peak-time delays of the prVEP with normal
amplitude most commonly signify conduction
delay but are not specic to demyelinating disease. In demyelinating disease, a conduction
delay can be observed even following the resolution of visual symptoms or, in some cases, may
show abnormality as a “clinically silent” lesion,
providing paraclinical evidence of demyelination
in conditions such as multiple sclerosis [1].
Importantly, peak-time delay is not specic to
demyelination but can be observed in various
optic nerve diseases, albeit to varying degrees.
Typically, with severe forms of demyelinating
optic neuropathies, PERG N95 loss and amplitude reduction of the VEP following the acute
phase are often associated with poorer visual outcomes (Fig.32.4).
While peak-time delay is most common, in
some pathologies, one can expect an atypically
early peak-time. Such abnormalities are usually
associated with an alteration in waveform morphology, such as bid or double-peaked waveform, discussed in the “shape” analysis below.
32.4.2 Amplitude
Reduced amplitude of a VEP suggests poor signal strength; as such, this is associated with macular pathway dysfunction. Reduced amplitude is
also a relatively non-specic indication of macular pathway abnormality. It is often observed in
conditions with reduced physiological signal
generation; for example, this may be reduced in
retinal disease, optic atrophy (whereby fewer
axons are functioning), or optic nerve hypoplasia. It is benecial to record pattern VEPs to
larger check widths to observe the alterations
with changes in spatial frequency. Recording to
a range of check widths is also useful, as it can
help with the monitoring of the disease, whereas
those for standard or small checks may progressively diminish in amplitude; therefore, the
larger check widths may sometimes be the only
means by which disease progression can be
monitored [13].
While reduced amplitudes are most commonly observed in diseases of the macular pathway, in rarer circumstances, VEPs may be
atypically large or “giant.” This may occur with
normal peak-time of the response in patients with
chronically raised intracranial pressure, perhaps
due to thinning of the skull, reduced cerebrospinal uid thickness, or cortical hyperexcitability
[14]. Similarly, atypically large VEPs can occur
with cortical hyperexcitability in epileptic disorders such as neuronal ceroid lipofuscinosis battens disease, where a “spike and wave” type
paroxysmal VEP response is observed, often with
an early peak-time [15]. In such circumstances,
VEP testing may be halted to minimize the risk
of pattern or ash-related seizure induction.
The pattern VEP can be a useful addition in
monitoring retinal disease, particularly in those
with rod–cone photoreceptor dystrophies. As
eld size reduces from the periphery and
encroaches upon the macula, the full-eld ERG
can be reduced or extinguished, albeit with vestigial PERG responses. As the fovea is often more
preserved during the later disease stages, the
prVEP recorded to a range of check widths can
provide information on the remaining integrity of
the macular pathway and be used for monitoring
disease progression. This is likely due to the
expanded foveal representation of the PVEP due
to cortical magnication, but it is particularly
useful to apply this when the ERG or PERG is
extinguished to provide a functional outcome
measure in disease [16]. An example of this is
shown in Fig.32.5.
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Fig. 32.4 An example of the waveforms seen in a patient
with left eye (LE) optic neuritis is associated with myelin
oligodendrocyte glycoprotein antibody-associated disease
(MOGAD). The normal waveforms of the pattern ERG,
VEP, and ash VEP are shown in the top panels. The
patient’s (unaffected) right eye (RE) shows normal PERG
ndings, with normal prVEP to large and small check
32.4.3 Shape
The morphology of the VEP can be altered in disease states and so can be used to delineate visual
pathway dysfunction. The most common abnormality in the VEP is a broadened or bid VEP
waveform.
A broadened prVEP can occur with macular
pathway abnormalities, likely due to temporal
dispersion of the afferent signal to the striate cortex. This has been reported in grading schemes of
VEPs in craniosynostosis [13], alongside other
pathologies. This has been proposed as a
widths and normal ash VEP. The patient’s affected LE
shows N95 amplitude loss and shortening of P50 peaktime, associated with retinal ganglion cell dysfunction.
The patient’s prVEP is reduced and delayed in the LE
relative to the RE to both large and small check widths.
The ash VEP is slightly simplied relative to the RE but
is of similar amplitude and peak-time
waveform N75-N135 peak-time difference
exceeding 90ms [13, 17]. The signicance of a
broadened prVEP likely reects mild macular
pathway dysfunction in the absence of amplitude
or peak- time anomalies. Nonetheless, these
changes are worth monitoring as they may suggest an early manifestation of visual pathway
dysfunction.
A bid VEP is a waveform which adopts a
P-N-P morphology, opposite to the typical conguration of N-P-N.This can be associated with
optic nerve or demyelinating disease, and it is the
author’s experience that these changes are due to
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Fig. 32.5 Electrophysiological ndings in a patient with
retinitis pigmentosa. The full-eld ERGs show severely
reduced DA a - and b-wave amplitudes, with preserved
but signicantly reduced amplitudes of the LA conemediated responses indicative of severe rod–cone dystrophy. The pattern ERG was reduced, and the amplitude did
not increase substantially between the 15° and 30° elds,
indicating distal retinal (cone-driven) dysfunction affect-
ing the 15°–30° eld. Despite these ndings, the prVEPs
and fVEPs are within the reference range. The ultrawideeld (Optos) fundus autouorescence shows pigmentary changes in the periphery (red arrow) alongside a
hyperuorescent ring around the macula. The macular
OCT shows IS/OS loss around the macular periphery,
with relative foveal sparing. The preservation of the
prVEPs is likely due to the relative foveal sparing
Fig. 32.6 The prVEPs in a healthy participant were
recorded with increasing central scotoma size (0–20°).
The waveform alterations can be observed with increasing
scotoma size to exhibit a bid morphology of the wave-
an enhancement of the paramacular prVEP components and a reduction of the major P100 peak
[12]. Accordingly, the nding of a bid prVEP
often suggests reduced central eld sensitivity or
central scotoma, meaning that the paramacular
retinal generators predominate the resultant
form with two positive peaks (red arrows). These peaks
correspond to the paramacular components of the halfeld prVEP (right panel, red arrow)
VEP. This is illustrated in Fig.32.6 in a healthy
individual; an increasingly larger scotoma alters
the prVEP morphology to adopt a bid waveform. As can also be seen, this waveform is similar to the paramacular components (p80) observed
contralaterally in the half-eld prVEP. As such,
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Fig. 32.7 Electrophysiological ndings in a patient with
Leber's hereditary optic neuropathy. The pattern ERG
shows early P50 peak-time and N95 amplitude loss indicating severe retinal ganglion cell disease. The prVEP
shows an abnormal morphology (red asterisk) with atypical bid morphology. The half-eld prVEPs show attenu-
recording half-eld prVEPs in patients with bid
prVEP waveforms helps one understand if these
components truly arise from a paramacular origin
or are caused by an alteration in the macular VEP
waveform (Fig.32.7).
32.4.4 Transoccipital Asymmetry
Transoccipital asymmetries can be investigated
when one extends the electrode montage to
include a multichannel recording. This typically
uses additional lateral electrodes, “O1” or “O2,”
according to the international 10–20 system. An
asymmetry across the occiput can dene transoccipital asymmetries. While individual laboratory
reference ranges will determine the limits for a
signicant transoccipital asymmetry (which may
depend on the check width and the eld size), it
is the author’s experience that a transoccipital
asymmetry (i.e., a difference between the lateral
electrodes) for an amplitude of >30% is considered suspicious, and those with amplitudes >50%
are considered signicant. Similarly, a peak-time
difference exceeding 6ms across the transoccipital array is also considered signicant.
A transoccipital asymmetry is typically suggestive of a chiasmal, post-chiasmal, or relative
eld defect, depending on the pattern of abnormality and if conrmed with appropriate testing.
The localization of the lesion can be achieved
ation of the ipsilateral major ip100 component (red
asterisks), yet the contralateral paramacular components
remain and correspond to the P80/P140 peaks observed in
the full-eld prVEP. This patient was later detected to
have a central scotoma on visual eld testing
with half-eld VEPs although knowledge of the
underlying neural substrates generating the
responses is crucial to determine the site of the
dysfunction accurately.
When using a large eld, with standard (or
large) check widths, with a mid-frontal reference
electrode, prVEPs demonstrate a phenomenon
known as paradoxical lateralization [18]. This
phenomenon means that responses generated to
the right half-eld stimulation (corresponding to
the left hemisphere) are “paradoxically” observed
over the right occipital electrode (Fig.32.6, right
panel). This is likely due to the oblique orientation of the cortical prVEP generators within the
calcarine sulcus. Conversely, pattern onset VEPs
do not exhibit paradoxical lateralization, yet pattern offset VEPs do, similar to prVEPs [19].
Abnormalities of the prVEP transoccipital distribution can therefore be elaborated upon using
half-eld stimulation of the left or right-half eld
of each eye. The abnormalities may be “crossed,”
meaning that the distribution of the transoccipital
asymmetry will be altered depending on which
eye is stimulated (e.g., in chiasmal dysfunction or
disproportion), or can be “un- crossed” in homonymous hemianopia (i.e., post- chiasmal
lesions). Half-eld testing can be used to elaborate on full-eld prVEP distributions, to identify
whether the transoccipital asymmetry is due to a
relative decit of one half-eld or whether this is
instead due to individual cortical architecture or
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Fig. 32.8 A patient with genetically conrmed oculocutaneous albinism. Data for the pattern onset (poVEP)
VEP, half-eld pattern reversal VEP (RHF prVEP/LHF
prVEP), and ash VEP are presented for electrodes overlaying the left occiput (left panels), right occiput (middle
panels), and a difference of these two (right panels). The
RE (red) and LE (blue) data are illustrated. The pattern
onset VEP shows that the major positive peak was largest
over the contralateral occiput, which when compared
VEP generator orientation. If half- eld testing is
not possible due to poor xation or cooperation,
the poVEP can be used to corroborate any potential eld defect. If the major pattern onset VEP
positivity is largest over the same lateral electrode as the prVEP, this likely reects individual
cortical architecture/VEP generator orientation,
whereas if the laterality is opposite between
from each eye in the difference channel shows a phase
reversal (red arrows). The half-eld prVEPs show a normal distribution of the bi-temporal elds but an atypically
symmetrical distribution of the bi-nasal elds. The fVEPs
show a clear difference in lateralization between eyes,
with a contralateral predominance of the major negativity
(~70ms) and positivity (~120ms) from each eye, which is
observed as a clear crossed asymmetry in the difference
channel (red arrows)
prVEPs and pattern onset VEPs, this is suggestive of a relative decit of a half-eld [19]. For
crossed asymmetries (i.e., where the direction of
the lateralization depends on the stimulated eye),
a virtual channel subtracting the difference
between the right and left occipital electrode is
useful to visualize the transoccipital symmetries
between the eyes (Fig.32.8). Some centers also
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perform a “chiasmal coefcient” calculation
[20], in which the difference between the left and
right electrodes from each eye are quantied for
a signicant correlation (negative or positive).
Such differences are usually utilized to investigate chiasmal misrouting associated with albinism although these may also be used to identify
patients with chiasmal dysfunction (i.e., spaceoccupying lesions or chiasmal hypoplasia).
32.5 Pitfalls andPearls
inRecording VEPs
The VEP can be an easily accessible and efcient
technique for assessing macular or generalized
pathway function and investigating visual pathway integrity. However, there are some circumstances where one must be aware of the limitations
or pitfalls of recording VEPs.
Perhaps one of the major misconceptions of the
VEP is that a normal VEP is equivalent to normal
sight. As the VEP only assesses the visual pathway
from the retina to the primary striate cortex, disorders of higher visual processing (e.g., cerebral
visual impairment) may not appear as abnormalities in the VEP.Similarly, the VEP cannot be used
in isolation to determine normal acuity in people
with functional disease. An otherwise normal
patient with organically reduced visual acuity
would be less likely to have a normal VEP.However,
it should be investigated with a sweep VEP to estimate visual acuity (Fig.32.9) objectively.
An important technical consideration for
recording the VEP is the importance of good xation and attention. The VEP can be easily altered
due to poor attention or xation on the stimulus.
Therefore, it is often advantageous to simultaneously monitor the patient’s xation with an infrared camera to perform intermittent averaging
(e.g., stimulus averaging is performed when the
patient’s xation is veried by viewing corneal
reections). This is particularly benecial in
pediatric or non-compliant people so that any
erroneous xation is accounted for when recording the VEP.
Lastly, an important note for recording the
VEP is to remain aware of the principles of VEP
signal acquisition. The VEP is an averaged
response from the time-locked background
EEG.As such, in people with abnormal posterior EEG activity (i.e., due to seizure disorders
or encephalopathies), the signal-to-noise ratio
of the VEP may be too poor to obtain a consistent or repeatable response. In such circumstances, the VEPs elicited can be easily
distinguished from erroneous EEG activity by
recording non- stimulus trials. To perform this,
one typically runs the VEP recording without
presenting a stimulus (i.e., by turning off the
monitor or facing the ash strobe down). If the
non-stimulus and stimulus trials are comparable, this suggests that any recorded waveform is
artifactual, whereas if these show a distinct difference, then it provides condence in its
authenticity.
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